Folia Microbiologica

, Volume 63, Issue 5, pp 645–651 | Cite as

Antibiotic resistance profiles of coagulase-positive and coagulase-negative staphylococci from pit latrine fecal sludge in a peri-urban South African community

  • Lorika S. Beukes
  • Stefan Schmidt
Original Article


The aim of this study was to assess pit latrine samples from a peri-urban community in KwaZulu-Natal (South Africa) for the presence of multidrug-resistant (MDR) Staphylococcus spp. Standard procedures were used to isolate Staphylococcus spp. from pit latrine fecal sludge samples, with confirmation at genus level by polymerase chain reaction (PCR). Sixty-eight randomly selected pit latrine Staphylococcus spp. isolates were further characterized by using established disk diffusion procedures. An average Staphylococcus spp. count of 2.1 × 105 CFU per g fecal material was established using two randomly selected pit latrine samples. Of the 68-selected Staphylococcus spp. pit latrine isolates, 49% were identified as coagulase positive, 51% as coagulase negative and 65% (12 coagulase positive, 32 coagulase negative isolates) were categorized as MDR. The majority (66/68) of Staphylococcus spp. isolates displayed resistance to fusidic acid while only 5/68 isolates displayed resistance to chloramphenicol. The pit latrine samples analyzed in this study are a source of MDR Staphylococcus spp., highlighting the need for proper hygiene and sanitation regimes in rural communities using these facilities.



British Society for Antimicrobial Chemotherapy


Colony-forming unit


Coagulase-negative staphylococcus


Coagulase-positive staphylococcus


European Committee on Antimicrobial Susceptibility Testing


International Organization for Standardization




Methicillin-resistant Staphylococcus aureus


Methicillin-susceptible Staphylococcus aureus


Oxacillin-resistant Staphylococcus aureus


Polymerase chain reaction



The authors would like to acknowledge the staff at Partners in Development (PiD) for their assistance in collecting the pit latrine samples and PiD/WRC (Water Research Commission) as well as the NRF (National Research Foundation) for financial support.

Compliance with ethical standards

Ethical clearance for this study was granted by the Humanities and Social Science Research Ethics Committee of the University of KwaZulu-Natal (ref. no. HSS/0653/013).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

12223_2018_605_MOESM1_ESM.pdf (125 kb)
ESM 1 (PDF 125 kb)


  1. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259CrossRefPubMedGoogle Scholar
  2. Ayepola OO, Olasupo NA, Egwari LO, Schaumburg F (2014) Antibiotic susceptibility pattern and biofilm formation in coagulase negative staphylococci. J Infect Dev Ctries 8:1643–1645CrossRefPubMedGoogle Scholar
  3. Becker K, Heilmann C, Peters G (2014) Coagulase-negative staphylococci. Clin Microbiol Rev 27:870–926CrossRefPubMedPubMedCentralGoogle Scholar
  4. Beukes LS, King TLB, Schmidt S (2017) Assessment of pit latrines in a peri-urban community in KwaZulu-Natal (South Africa) as a source of antibiotic resistant E. coli strains. Int J Hyg Environ Health 220:1279–1284CrossRefPubMedGoogle Scholar
  5. BSAC (British Society for Antimicrobial Chemotherapy) (2015a) BSAC methods for antimicrobial susceptibility testing. Version 14.0, 05-01-2015.
  6. BSAC (British Society for Antimicrobial Chemotherapy) (2015b) Standing committee on susceptibility testing - breakpoint tables. Version 14.0, 05-01-2015.
  7. Campillo B, Dupeyron C, Richardet JP (2001) Epidemiology of hospital-acquired infections in cirrhotic patients: effect of carriage of methicillin-resistant Staphylococcus aureus and influence of previous antibiotic therapy and norfloxacin prophylaxis. Epidemiol Infect 127:443–450CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chambers HF (2001) The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7:178–182CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cook N (1998) Methicillin-resistant Staphylococcus aureus versus the burn patient. Burns 24:91–98CrossRefPubMedGoogle Scholar
  10. Dudley DJ, Guentzel MN, Ibarra MJ, Moore BE, Sagik BP (1980) Enumeration of potentially pathogenic bacteria from sewage sludges. Appl Environ Microbiol 39:118–126PubMedPubMedCentralGoogle Scholar
  11. Dumontet S, Scopa A, Kerje S, Krovacek K (2001) The importance of pathogenic organisms in sewage and sewage sludge. J Air Waste Manag Assoc 51:848–860CrossRefPubMedGoogle Scholar
  12. von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2:677–685CrossRefGoogle Scholar
  13. EUCAST (European Committee on Antimicrobial Susceptibility Testing) (2015) Antimicrobial susceptibility testing EUCAST disk diffusion method. Version 5.0. 2015.
  14. EUCAST (European Committee on Antimicrobial Susceptibility Testing) (2016) Breakpoint tables for interpretation of MICs and zone diameters. Version 6.0. 2016
  15. Faria C, Vaz-Moreira I, Serapicos E, Nunes OC, Manaia CM (2009) Antibiotic resistance in coagulase negative staphylococci isolated from wastewater and drinking water. Sci Total Environ 407:3876–3882CrossRefPubMedGoogle Scholar
  16. Flemming K, Ackermann G (2007) Prevalence of enterotoxin producing Staphylococcus aureus in stools of patients with nosocomial diarrhea. Infection 35:356–358CrossRefPubMedGoogle Scholar
  17. Gemmell ME, Schmidt S (2013) Is the microbiological quality of the Msunduzi River (KwaZulu-Natal, South Africa) suitable for domestic, recreational, and agricultural purposes? Environ Sci Pollut Res 20:6551–6562CrossRefGoogle Scholar
  18. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE et al (2008) Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis 197:1226–1234CrossRefPubMedGoogle Scholar
  19. Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9:486–493CrossRefPubMedGoogle Scholar
  20. Irenge LM, Kabego L, Kinunu FB, Itongwa M, Mitangala PN, Gala J-L, Chirimwami RB (2015) Antimicrobial resistance of bacteria isolated from patients with bloodstream infections at a tertiary care hospital in the Democratic Republic of the Congo. S Afr Med J 105:752–755CrossRefPubMedGoogle Scholar
  21. ISO 6888–1 (1999) Microbiology of food and animal feeding stuffs: horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species). International Organization for Standardization, GenevaGoogle Scholar
  22. Jevons MP (1961) “Celbenin” resistant staphylococci. Br Med J 1:124–125CrossRefPubMedCentralGoogle Scholar
  23. Kanj SS, Whitelaw A, Dowzicky MJ (2014) In vitro activity of tigecycline and comparators against Gram-positive and Gram-negative isolates collected from the Middle East and Africa between 2004 and 2011. Int J Antimicrob Agents 43:170–178CrossRefPubMedGoogle Scholar
  24. Koksal F, Yasar H, Samasti M (2009) Antibiotic resistance patterns of coagulase negative staphylococcus strains isolated from blood cultures of septicemic patients in Turkey. Microbiol Res 164:404–410CrossRefPubMedGoogle Scholar
  25. Kumburu HH, Sonda T, Leekitcharoenphon P, van Zwetselaar M, Lukjancenko O, Alifrangis M, Lund O, Mmbaga BT, Kibiki G, Aarestrup FM (2018) Hospital epidemiology of methicillin-resistant Staphylococcus aureus in a tertiary care hospital in Moshi, Tanzania, as determined by whole genome sequencing. Biomed Res Int 2018:12–12. CrossRefGoogle Scholar
  26. Lindberg E, Adlerberth I, Matricardi P, Bonanno C, Tripodi S, Panetta V, Hesselmar B, Saalman R, Å berg N, Wold AE (2011) Effect of lifestyle factors on Staphylococcus aureus gut colonization in Swedish and Italian infants. Clin Microbiol Infect 17:1209–1215CrossRefPubMedGoogle Scholar
  27. Mainous AG, Hueston WJ, Everett CJ, Diaz VA (2006) Nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus in the United States, 2001-2002. Ann Fam Med 4:132–137CrossRefPubMedPubMedCentralGoogle Scholar
  28. Martineau F, Picard FJ, Danbing KE, Paradis S, Roy PH, Ouellette M, Bergeron MG (2001) Development of a PCR assay for identification of staphylococci at genus and species levels. J Clin Microbiol 39:2541–2547CrossRefPubMedPubMedCentralGoogle Scholar
  29. McKay R, Bamford C (2015) Community- versus healthcare-acquired bloodstream infections at Groote Schuur Hospital, Cape Town, South Africa. S Afr Med J 105:363–369CrossRefPubMedGoogle Scholar
  30. Mottola C, Semedo-Lemsaddek T, Mendes JJ, Melo-Cristino J, Tavares L, Cavaco-Silva P, Oliveira M (2016) Molecular typing, virulence traits and antimicrobial resistance of diabetic foot staphylococci. J Biomed Sci 23:33CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ndihokubwayo JB, Yahaya AA, Desta AT, Ki-Zerbo G, Odei EA, Keita B et al (2013) Antimicrobial resistance in the African region: issues, challenges and actions proposed. African Health Monitor 16:27–30Google Scholar
  32. Ntirenganya C, Manzi O, Muvunyi CM, Ogbuagu O (2015) High prevalence of antimicrobial resistance among common bacterial isolates in a tertiary healthcare facility in Rwanda. Am J Trop Med Hyg 92:865–870CrossRefPubMedPubMedCentralGoogle Scholar
  33. Otto M (2009) Staphylococcus epidermidis—the “accidental” pathogen. Nat Rev Microbiol 7:555–567CrossRefPubMedPubMedCentralGoogle Scholar
  34. Otto M (2013) Community-associated MRSA: what makes them special? Int J Med Microbiol 303:324–330CrossRefPubMedPubMedCentralGoogle Scholar
  35. Petinaki E, Spiliopoulou I, Maniati M, Maniatis AN (2005) Emergence of Staphylococcus hominis strains expressing low-level resistance to quinupristin/dalfopristin in Greece. J Antimicrob Chemother 55:811–812CrossRefPubMedGoogle Scholar
  36. Pinho MG, Filipe SR, de Lencastres H, Tomasz A (2001) Complementation of the essential peptidoglycan transpeptidase function of penicillin-binding protein 2 (PBP2) by drug resistance protein PBP2A in Staphylococcus aureus. J Bacteriol 183:6525–6531CrossRefPubMedPubMedCentralGoogle Scholar
  37. Schmidt VM, Williams NJ, Pinchbeck G, Corless CE, Shaw S, McEwan N, Dawson S, Nuttall T (2014) Antimicrobial resistance and characterization of staphylococci isolated from healthy Labrador retrievers in the United Kingdom. BMC Vet Res 10:17CrossRefPubMedPubMedCentralGoogle Scholar
  38. Schulz J, Friese A, Klees S, Tenhagen BA, Fetsch A, Rosler U et al (2012) Longitudinal study of the contamination of air and of soil surfaces in the vicinity of pig barns by livestock-associated methicillin-resistant Staphylococcus aureus. Appl Environ Microbiol 78:5666–5671CrossRefPubMedPubMedCentralGoogle Scholar
  39. Shittu AO, Lin J (2006) Antimicrobial susceptibility patterns and characterization of clinical isolates of Staphylococcus aureus in KwaZulu-Natal province, South Africa. BMC Infect Dis 6:125CrossRefPubMedPubMedCentralGoogle Scholar
  40. Szczuka E, Makowska N, Bosacka K, Słotwińska A, Kaznowski A (2016) Molecular basis of resistance to macrolides, lincosamides and streptogramins in Staphylococcus hominis strains isolated from clinical specimens. Folia Microbiol 61:143–147CrossRefGoogle Scholar
  41. Tsuji BT, Rybak MJ, Cheung CM, Amjad M, Kaatz GW (2007) Community- and health care-associated methicillin-resistant Staphylococcus aureus: a comparison of molecular epidemiology and antimicrobial activities of various agents. Diagn Microbiol Infect Dis 58:41–47CrossRefPubMedGoogle Scholar
  42. Visser A, Moore DP, Whitelaw A, Lowman W, Kantor G (2011) Global antibiotic resistance partnership, situation analysis: antibiotic use and resistance in South Africa—part VII: interventions. South Afr Med J 101:587–595Google Scholar
  43. WHO (World Health Organization) (2001) WHO global strategy for containment of antimicrobial resistance. WHO/CDS/CSR/DRS/2001.2: 2001. Accessed 12 Apr 2017
  44. WHO (World Health Organization) (2017a) Progress on drinking water, sanitation and hygiene: 2017 update and SDG baselines. World Health Organization (WHO) and the United Nations Children’s Fund (UNICEF), GenevaGoogle Scholar
  45. WHO (World Health Organization) (2017b) WHO model list of essential medicines, 20th Ed. World Health Organization, GenevaGoogle Scholar
  46. Wright GD, Poinar H (2012) Antibiotic resistance is ancient: implications for drug discovery. Trends Microbiol 20:157–159CrossRefPubMedGoogle Scholar
  47. York MK, Gibbs L, Chehab F, Brooks GF (1996) Comparison of PCR detection of mecA with standard susceptibility testing methods to determine methicillin resistance in coagulase-negative staphylococci. J Clin Microbiol 34:249–253PubMedPubMedCentralGoogle Scholar
  48. Youn J-H, Park YH, Hang’ombec B, Sugimoto C (2014) Prevalence and characterization of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from companion animals and environment in the veterinary teaching hospital in Zambia, Africa. Comp Immunol Microbiol Infect Dis 37:123–130CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2018

Authors and Affiliations

  1. 1.Discipline of Microbiology, School of Life SciencesUniversity of KwaZulu-NatalPietermaritzburgSouth Africa

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